Sodium dodecyl sulfate-coated silver nanoparticles accelerate antimicrobial potentials by targeting amphiphilic membranes

Xiuyan Jin , Na Peng , Aoran Cui , Yue Liu , Xianqi Peng , Linlin Huang , Abdelaziz Ed-Dra , Fang He , Yan Li , Shikuan Yang , Min Yue

mLife ›› 2024, Vol. 3 ›› Issue (4) : 551 -564.

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mLife ›› 2024, Vol. 3 ›› Issue (4) : 551 -564. DOI: 10.1002/mlf2.12143
ORIGINAL RESEARCH

Sodium dodecyl sulfate-coated silver nanoparticles accelerate antimicrobial potentials by targeting amphiphilic membranes

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Abstract

Compelling concerns about antimicrobial resistance and the emergence of multidrug-resistant pathogens call for novel strategies to address these challenges. Nanoparticles show promising antimicrobial activities; however, their actions are hindered primarily by the bacterial hydrophilic–hydrophobic barrier. To overcome this, we developed a method of electrochemically anchoring sodium dodecyl sulfate (SDS) coatings onto silver nanoparticles (AgNPs), resulting in improved antimicrobial potency. We then investigated the antimicrobial mechanisms and developed therapeutic applications. We demonstrated SDS-coated AgNPs with anomalous dispersive properties capable of dispersing in both polar and nonpolar solvents and, further, detected significantly higher bacteriostatic and bactericidal effects compared to silver ions (Ag+). Cellular assays suggested multipotent disruptions targeting the bacterial membrane, evidenced by increasing lactate dehydrogenase, protein and sugar leakage, and consistent with results from the transcriptomic analysis. Notably, the amphiphilic characteristics of the AgNPs maintained robust antibacterial activities for a year at various temperatures, indicating long-term efficacy as a potential disinfectant. In a murine model, the AgNPs showed considerable biocompatibility and could alleviate fatal Salmonella infections. Collectively, by gaining amphiphilic properties from SDS, we offer novel AgNPs against bacterial infections combined with long-term and cost-effective strategies.

Keywords

amphiphilic properties / antimicrobial agents / antimicrobial resistance / feed additive / silver nanoparticles

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Xiuyan Jin, Na Peng, Aoran Cui, Yue Liu, Xianqi Peng, Linlin Huang, Abdelaziz Ed-Dra, Fang He, Yan Li, Shikuan Yang, Min Yue. Sodium dodecyl sulfate-coated silver nanoparticles accelerate antimicrobial potentials by targeting amphiphilic membranes. mLife, 2024, 3(4): 551-564 DOI:10.1002/mlf2.12143

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References

[1]

Prestinaci F, Pezzotti P, Pantosti A. Antimicrobial resistance: a global multifaceted phenomenon. Pathog Glob Health. 2015;109:309–318.

[2]

Murray C, Ikuta KS, Sharara F, Swetschinski L, Robles Aguilar G, Gray A, et al. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. Lancet. 2022;399:629–655.

[3]

Jia C, Wang Z, Huang C, Teng L, Zhou H, An H, et al. Mobilome-driven partitions of the resistome in Salmonella. mSystems. 2023;8:e00883-23.

[4]

Wang Z, Huang C, Liu Y, Chen J, Yin R, Jia C, et al. Salmonellosis outbreak archive in China: data collection and assembly. Sci Data. 2024;11:244.

[5]

Wang Z, Zhou H, Liu Y, Huang C, Chen J, Siddique A, et al. Nationwide trends and features of human salmonellosis outbreaks in China. Emerg Microbes Infect. 2024;13:2372364.

[6]

Huang L, Zhou H, Chen J, Jia C, Siddique A, Wu B, et al. Impact of COVID-19-related nonpharmaceutical interventions on diarrheal diseases and zoonotic Salmonella. hLife. 2024;2:246–256.

[7]

World Health Organization. Antimicrobial resistance. World Health Organization Official Website. 2023 [cited 2024 Jan 15]. https://www.who.int/news-room/fact-sheets/detail/antimicrobial-resistance

[8]

EClinicalMedicine. Antimicrobial resistance: a top ten global public health threat. EClinicalMed. 2021;41:101221.

[9]

Ke Y, Teng L, Zhu Z, Lu W, Liu W, Zhou H, et al. Genomic investigation and nationwide tracking of pediatric invasive nontyphoidal Salmonella in China. mLife. 2024;3:156–160.

[10]

Feng Y, Pan H, Zheng B, Li F, Teng L, Jiang Z, et al. An integrated nationwide genomics study reveals transmission modes of typhoid fever in China. mBio. 2023;14:e0133323.

[11]

Zhou X, Kang X, Chen J, Song Y, Jia C, Teng L, et al. Genome degradation promotes Salmonella pathoadaptation by remodeling fimbriae-mediated proinflammatory response. Natl Sci Rev. 2023;10:nwad228.

[12]

Li Y, Teng L, Xu X, Li X, Peng X, Zhou X, et al. A nontyphoidal Salmonella serovar domestication accompanying enhanced niche adaptation. EMBO Mol Med. 2022;14:e16366.

[13]

Paudyal N, Pan H, Wu B, Zhou X, Zhou X, Chai W, et al. Persistent asymptomatic human infections by Salmonella enterica serovar Newport in China. mSphere. 2020;5:00163-20.

[14]

Orta-Rivera AM, Meléndez-Contés Y, Medina-Berríos N, Gómez-Cardona AM, Ramos-Rodríguez A, Cruz-Santiago C, et al. Copper-based antibiotic strategies: exploring applications in the hospital setting and the targeting of Cu regulatory pathways and current drug design trends. Inorganics. 2023;11:252.

[15]

Peng X, Ed-Dra A, Song Y, Elbediwi M, Nambiar RB, Zhou X, et al. Lacticaseibacillus rhamnosus alleviates intestinal inflammation and promotes microbiota-mediated protection against Salmonella fatal infections. Front Immunol. 2022;13:973224.

[16]

Moorthy K, Chang K-C, Yang H-H, Su W-M, Chiang C-K, Yuan Z. Recent developments in detection and therapeutic approaches for antibiotic-resistant bacterial infections. J Food Drug Anal. 2023;31:1–19.

[17]

Ivask A, ElBadawy A, Kaweeteerawat C, Boren D, Fischer H, Ji Z, et al. Toxicity mechanisms in Escherichia coli vary for silver nanoparticles and differ from Ionic silver. ACS Nano. 2014;8:374–386.

[18]

Seong M, Lee DG. Silver nanoparticles against Salmonella enterica serotype Typhimurium: role of inner membrane dysfunction. Curr Microbiol. 2017;74:661–670.

[19]

Chaloupka K, Malam Y, Seifalian AM. Nanosilver as a new generation of nanoproduct in biomedical applications. Trends Biotechnol. 2010;28:580–588.

[20]

Hamida RS, Ali MA, Goda DA, Khalil MI, Al-Zaban MI. Novel biogenic silver nanoparticle-induced reactive oxygen species inhibit the biofilm formation and virulence activities of methicillin-resistant Staphylococcus aureus (MRSA) strain. Front Bioeng Biotechnol. 2020;8:433.

[21]

Quinteros MA, Cano Aristizábal V, Dalmasso PR, Paraje MG, Páez PL. Oxidative stress generation of silver nanoparticles in three bacterial genera and its relationship with the antimicrobial activity. Toxicol In Vitro. 2016;36:216–223.

[22]

Tripathi N, Goshisht MK. Recent advances and mechanistic insights into antibacterial activity, antibiofilm activity, and cytotoxicity of silver nanoparticles. ACS Appl Bio Mater. 2022;5:1391–1463.

[23]

Butler J, Handy RD, Upton M, Besinis A. Review of antimicrobial nanocoatings in medicine and dentistry: mechanisms of action, biocompatibility performance, safety, and benefits compared to antibiotics. ACS Nano. 2023;17:7064–7092.

[24]

Slavin YN, Asnis J, Häfeli UO, Bach H. Metal nanoparticles: understanding the mechanisms behind antibacterial activity. J Nanobiotechnol. 2017;15:65.

[25]

Liu Y, Peng N, Yao Y, Zhang X, Peng X, Zhao L, et al. Breaking the nanoparticle’s dispersible limit via rotatable surface ligands. Nat Commun. 2022;13:3581.

[26]

Wu K, Li H, Cui X, Feng R, Chen W, Jiang Y, et al. Mutagenesis and resistance development of bacteria challenged by silver nanoparticles. Antimicrob Agents Chemother. 2022;66:e00628-22.

[27]

Panáček A, Kvítek L, Smékalová M, Večeřová R, Kolář M, Röderová M, et al. Bacterial resistance to silver nanoparticles and how to overcome it. Nat Nanotechnol. 2018;13:65–71.

[28]

Chen Q, Zhao L, Liu H, Ding Q, Jia C, Liao S, et al. Nanoporous silver nanorods as surface-enhanced Raman scattering substrates. Biosens Bioelectron. 2022;202:114004.

[29]

Hussain Z, Lannigan R, Schieven BC, Stoakes L, Groves D. Comparison of susceptibility results of anaerobic organisms determined by agar dilution method and sceptor anaerobe MIC/ID micro broth dilution panels. Diagn Microbiol Infect Dis. 1987;8:95–100.

[30]

Parvekar P, Palaskar J, Metgud S, Maria R, Dutta S. The minimum inhibitory concentration (MIC) and minimum bactericidal concentration (MBC) of silver nanoparticles against Staphylococcus aureus. Biomater Invest Dent. 2020;7:105–109.

[31]

Santajit S, Indrawattana N. Mechanisms of antimicrobial resistance in ESKAPE pathogens. BioMed Res Int. 2016;2475067.

[32]

Gallo M, Ferrara L, Calogero A, Montesano D, Naviglio D. Relationships between food and diseases: what to know to ensure food safety. Food Res Int. 2020;137:109414.

[33]

Pasquina-Lemonche L, Burns J, Turner RD, Kumar S, Tank R, Mullin N, et al. The architecture of the gram-positive bacterial cell wall. Nature. 2020;582:294–297.

[34]

Rojas ER, Billings G, Odermatt PD, Auer GK, Zhu L, Miguel A, et al. The outer membrane is an essential load-bearing element in gram-negative bacteria. Nature. 2018;559:617–621.

[35]

Roy A. Hairy root culture an alternative for bioactive compound production from medicinal plants. Curr Pharm Biotechnol. 2020;22:136–149.

[36]

Akter S, Huq MA. Biologically rapid synthesis of silver nanoparticles by Sphingobium sp. MAH-11T and their antibacterial activity and mechanisms investigation against drug-resistant pathogenic microbes. Artif Cells, Nanomed, Biotechnol. 2020;48:672–682.

[37]

Algebaly AS, Mohammed AE, Abutaha N, Elobeid MM. Biogenic synthesis of silver nanoparticles: antibacterial and cytotoxic potential. Saudi J Biol Sci. 2020;27:1340–1351.

[38]

Liao S, Zhang Y, Pan X, Zhu F, Jiang C, Liu Q, et al. Antibacterial activity and mechanism of silver nanoparticles against multidrug-resistant Pseudomonas aeruginosa. Int J Nanomed. 2019;14:1469–1487.

[39]

Kang X, An H, Wang B, Huang L, Huang C, Huang Y, et al. Integrated OMICs approach reveals energy metabolism pathway is vital for Salmonella Pullorum survival within the egg white. mSphere. 2024;9:e00362-24.

[40]

Kumar P, Nagarajan A, Uchil PD. Analysis of cell viability by the lactate dehydrogenase assay. Cold Spring Harbor Protocols. 2018;2018:pdb.prot095497.

[41]

Hamida RS, Ali MA, Goda DA, Khalil MI, Redhwan A. Cytotoxic effect of green silver nanoparticles against ampicillin-resistant Klebsiella pneumoniae. RSC Adv. 2020;10:21136–21146.

[42]

Mohd Yusof H, Abdul Rahman N, Mohamad R, Hasanah Zaidan U, Samsudin AA. Antibacterial potential of biosynthesized zinc oxide nanoparticles against poultry-associated foodborne pathogens: an in vitro study. Animals. 2021;11:2093.

[43]

Kim S. Antibacterial activity of silver-nanoparticles against Staphylococcus aureus and Escherichia coli. Korean J Microbiol Biotechnol. 2011;39:77–85.

[44]

Silhavy TJ, Kahne D, Walker S. The bacterial cell envelope. Cold Spring Harbor Perspect Biol. 2010;2:a000414.

[45]

Hamida RS, Ali MA, Goda DA, Al-Zaban MI. Lethal mechanisms of Nostoc-synthesized silver nanoparticles against different pathogenic bacteria. Int J Nanomed. 2020;15:10499–10517.

[46]

Seeger MA, van Veen HW. Molecular basis of multidrug transport by ABC transporters. Biochim Biophys Acta Prot Proteom. 2009;1794:725–737.

[47]

Banerjee M, Mallick S, Paul A, Chattopadhyay A, Ghosh SS. Heightened reactive oxygen species generation in the antimicrobial activity of a three component iodinated chitosan−silver nanoparticle composite. Langmuir. 2010;26:5901–5908.

[48]

Gurunathan S, Choi Y-J, Kim J-H. Antibacterial efficacy of silver nanoparticles on endometritis caused by Prevotella melaninogenica and Arcanobacterum pyogenes in dairy cattle. Int J Mol Sci. 2018;19:1210.

[49]

Hou J, Zhao L, Tang H, He X, Ye G, Shi F, et al. Silver nanoparticles induced oxidative stress and mitochondrial injuries mediated autophagy in HC11 cells through Akt/AMPK/mTOR pathway. Biol Trace Elem Res. 2021;199:1062–1073.

[50]

Masip L, Veeravalli K, Georgiou G. The many faces of glutathione in bacteria. Antioxid Redox Signal. 2006;8:753–762.

[51]

Yuan Y-G, Cai H-Q, Wang J-L, Mesalam A, Md Talimur Reza AM, Li L, et al. Graphene oxide–silver nanoparticle nanocomposites induce oxidative stress and aberrant methylation in caprine fetal fibroblast cells. Cells. 2021;10:682.

[52]

Bueno R, Braga R, Segretti N, Ferreira E, Trossini G, Andrade C, et al. New tuberculostatic agents targeting nucleic acid biosynthesis: drug design using qsar approaches. Curr Pharm Des. 2013;20:4474–4485.

[53]

Rowlett VW, Mallampalli VKPS, Karlstaedt A, Dowhan W, Taegtmeyer H, Margolin W, et al. Impact of membrane phospholipid alterations in Escherichia coli on cellular function and bacterial stress adaptation. J Bacteriol. 2017;199:e00849-16.

[54]

Dalebroux ZD. Cues from the membrane: bacterial glycerophospholipids. J Bacteriol. 2017;199:e00136-17.

[55]

de Carvalho C, Caramujo M. The various roles of fatty acids. Molecules. 2018;23:2583.

[56]

Jimenez-Diaz L, Caballero A, Segura A. Aerobic utilization of hydrocarbons, oils and lipids. In: Rojo F, editor. Pathways for the degradation of fatty acids in bacteria. Springer Nature. p. 1–23.

[57]

Kaynar MY, Hanci M, Kuday C, Belce A, Gumustas K, Kokoglu E. Changes in the activity of antioxidant enzymes (SOD, GPX, CAT) after experimental spinal cord injury. Tokushima J Exp Med. 1994;41:133–136.

[58]

Ahmad T, Mahbood F, Sarwar R, Iqbal A, Khan M, Muhammad S, et al. Synthesis of gemifloxacin conjugated silver nanoparticles, their amplified bacterial efficacy against human pathogen and their morphological study via TEM analysis. Artif Cells Nanomed Biotechnol. 2021;49:661–671.

[59]

Kage H, Takaya A, Ohya M, Yamamoto T. Coordinated regulation of expression of Salmonella pathogenicity island 1 and flagellar type III secretion systems by ATP-dependent ClpXP protease. J Bacteriol. 2008;190:2470–2478.

[60]

CDC. Antibiotic resistance threats in the United States, 2019. Atlanta, GA: US.: Department of Health and Human Services, CDC; 2019.

[61]

World Health Organization. Salmonella (non-typhoidal). World Health Organization Official Website. 2018 [cited 2024 Jan 15]. https://www.who.int/news-room/fact-sheets/detail/salmonella-(non-typhoidal)

[62]

Galán JE. Salmonella Typhimurium and inflammation: a pathogen-centric affair. Nat Rev Microbiol. 2021;19:716–725.

[63]

Biswas S, Li Y, Elbediwi M, Yue M. Emergence and dissemination of mcr-carrying clinically relevant Salmonella Typhimurium monophasic clone ST34. Microorganisms. 2019;7:298.

[64]

Gopinath S, Carden S, Monack D. Shedding light on Salmonella carriers. TIM. 2012;20:320–327.

[65]

Paudyal N, Yue M. Antimicrobial resistance in the “Dark Matter”. Clin Infect Dis. 2019;69:379–380.

[66]

Xu X, Biswas S, Gu G, Elbediwi M, Li Y, Yue M. Characterization of multidrug resistance patterns of emerging Salmonella enterica serovar rissen along the food chain in China. Antibiotics. 2020;9:660.

[67]

Dunlap NE, Benjamin WH, McCall RD, Tilden AB, Briles DE. A “safe-site” for Salmonella typhimurium is within splenic cells during the early phase of infection in mice. Microb Pathog. 1991;10:297–310.

[68]

Liu J, Huang H, Yang Q, Zhao J, Zhang H, Chen W, et al. Dietary supplementation of n-3LCPUFAs prevents salmonellosis in a murine model. J Agricult Food Chem. 2020;68:128–137.

[69]

Farouk MM, El-Molla A, Salib FA, Soliman YA, Shaalan M. The role of silver nanoparticles in a treatment approach for multidrug-resistant Salmonella species isolates. Int J Nanomedicine. 2020;15:6993–7011.

[70]

Zu M, Xie D, Canup BSB, Chen N, Wang Y, Sun R, et al. ‘Green’ nanotherapeutics from tea leaves for orally targeted prevention and alleviation of colon diseases. Biomaterials. 2021;279:121178.

[71]

Li Y, Ed-Dra A, Tang B, Kang X, Müller A, Kehrenberg C, et al. Higher tolerance of predominant Salmonella serovars circulating in the antibiotic-free feed farms to environmental stresses. J Hazard Mater. 2022;438:129476.

[72]

Afsharzadeh M, Naderinasab M, Tayarani Najaran Z, Barzin M, Emami SA. In-vitro antimicrobial activities of some Iranian conifers. Iran J Pharmaceut Res. 2013;12:63–74.

[73]

Romero-Urbina DG, Lara HH, Velázquez-Salazar JJ, Arellano-Jiménez MJ, Larios E, Srinivasan A, et al. Ultrastructural changes in methicillin-resistant Staphylococcus aureus induced by positively charged silver nanoparticles. Beilstein J Nanotechnol. 2015;6:2396–2405.

[74]

Deshavath NN, Mukherjee G, Goud VV, Veeranki VD, Sastri CV. Pitfalls in the 3, 5-dinitrosalicylic acid (DNS) assay for the reducing sugars: interference of furfural and 5-hydroxymethylfurfural. Int J Biiol Macromol. 2020;156:180–185.

[75]

Paudyal N, Pan H, Elbediwi M, Zhou X, Peng X, Li X, et al. Characterization of Salmonella Dublin isolated from bovine and human hosts. BMC Microbiol. 2019;19:226.

[76]

Robinson MD, McCarthy DJ, Smyth GK. EdgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26:139–140.

[77]

Anders S, Pyl PT, Huber W. HTSeq: a python framework to work with high-throughput sequencing data. Bioinformatics. 2015;31:166–169.

[78]

Pertea M, Kim D, Pertea GM, Leek JT, Salzberg SL. Transcript-level expression analysis of RNA-seq experiments with hisat, stringtie and ballgown. Nat Protoc. 2016;11:1650–1667.

[79]

Pertea M, Pertea GM, Antonescu CM, Chang T-C, Mendell JT, Salzberg SL. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol. 2015;33:290–295.

[80]

Yu G, Wang L-G, Han Y, He Q-Y. ClusterProfiler: an R package for comparing biological themes among gene clusters. OMICS J Integr Biol. 2012;16:284–287.

[81]

Wu J, Pugh R, Laughlin RC, Andrews-Polymenis H, McClelland M, Bäumler AJ, et al. High-throughput assay to phenotype Salmonella enterica Typhimurium association, invasion, and replication in macrophages. JoVE. 2014;90:51759.

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2024 The Author(s). mLife published by John Wiley & Sons Australia, Ltd on behalf of Institute of Microbiology, Chinese Academy of Sciences.

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